Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

Nicole S Paulat; Jessica M Storer; Diana D Moreno-Santillán; Austin B Osmanski; Kevin A M Sullivan; Jenna R Grimshaw; Jennifer Korstian; Michaela Halsey; Carlos J Garcia; Claudia Crookshanks; Jaquelyn Roberts; Arian F A Smit; Robert Hubley; Jeb Rosen; Emma C Teeling; Sonja C Vernes; Eugene Myers; Martin Pippel; Thomas Brown; Michael Hiller; Zoonomia Consortium; Danny Rojas; Liliana M Dávalos; Kerstin Lindblad-Toh; Elinor K Karlsson; David A Ray

doi:10.1093/molbev/msad092

Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

Nicole S Paulat, Jessica M Storer, Diana D Moreno-Santillán, Austin B Osmanski, Kevin A M Sullivan, Jenna R Grimshaw, Jennifer Korstian, Michaela Halsey, Carlos J Garcia, Claudia Crookshanks, Jaquelyn Roberts, Arian F A Smit, Robert Hubley, Jeb Rosen, Emma C Teeling, Sonja C Vernes, Eugene Myers, Martin Pippel, Thomas Brown, Michael HillerZoonomia Consortium, Danny Rojas, Liliana M Dávalos, Kerstin Lindblad-Toh, Elinor K Karlsson, David A Ray^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

Original language	English
Article number	msad092
Number of pages	14
Journal	Molecular Biology and Evolution
Volume	40
Issue number	5
Early online date	18 Apr 2023
DOIs	https://doi.org/10.1093/molbev/msad092
Publication status	Published - 1 May 2023

Keywords

Fusogenic envelope protein
Platypus
Endogenous retrovirus
Echidna
Monotremes

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10.1093/molbev/msad092Licence: CC BY-NC

Paulat_2023_MBE_Chiropterans-hotspots_CC
Copyright © The Author(s) 2023. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Final published version, 1.84 MBLicence: CC BY-NC

Sonja Vernes UKRI Future Leaders: Mammalian vocal communication as a model for human language; from genes and brains to behaviour
Vernes, S. (PI)
UK Research and Innovation
1/11/20 → 31/10/25
Project: Fellowship

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Paulat, N. S., Storer, J. M., Moreno-Santillán, D. D., Osmanski, A. B., Sullivan, K. A. M., Grimshaw, J. R., Korstian, J., Halsey, M., Garcia, C. J., Crookshanks, C., Roberts, J., Smit, A. F. A., Hubley, R., Rosen, J., Teeling, E. C., Vernes, S. C., Myers, E., Pippel, M., Brown, T., ... Ray, D. A. (2023). Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia. Molecular Biology and Evolution, 40(5), Article msad092. https://doi.org/10.1093/molbev/msad092

@article{0dd12c714adf426ea097af3f429aad64,

title = "Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia",

abstract = "Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.",

keywords = "Fusogenic envelope protein, Platypus, Endogenous retrovirus, Echidna, Monotremes",

author = "Paulat, {Nicole S} and Storer, {Jessica M} and Moreno-Santill{\'a}n, {Diana D} and Osmanski, {Austin B} and Sullivan, {Kevin A M} and Grimshaw, {Jenna R} and Jennifer Korstian and Michaela Halsey and Garcia, {Carlos J} and Claudia Crookshanks and Jaquelyn Roberts and Smit, {Arian F A} and Robert Hubley and Jeb Rosen and Teeling, {Emma C} and Vernes, {Sonja C} and Eugene Myers and Martin Pippel and Thomas Brown and Michael Hiller and Zoonomia Consortium and Danny Rojas and D{\'a}valos, {Liliana M} and Kerstin Lindblad-Toh and Karlsson, {Elinor K} and Ray, {David A}",

note = "Funding: This project was supported by the National Science Foundation (grant numbers DEB 1838283 and IOS 2032006 to D.M.-S. and Dav.R. and DEB 1838273 and DGE 1633299 to L.D.), National Institutes of Health (grant numbers R01HG002939 and U24HG010136 to J.S., R.H., A.F.A.S., and Je.R.), NHGRI (grant number R01HG008742 to Z.C.), Irish Research Council (grant number IRCLA/ 2017/58 to E.T.), Science Foundation Ireland (grant number 19/FFP/6790 to E.T.), Max Planck Research Group awarded by the Max Planck Gesellschaft to S.V., Human Frontiers Science Program (grant number RGP0058/2016 to S.V.), UK Research and Innovation (grant number MR/T021985/1 to S.V.), and the Swedish Research Council Distinguished Professor Award to K.L.-T.",

year = "2023",

month = may,

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doi = "10.1093/molbev/msad092",

language = "English",

volume = "40",

journal = "Molecular Biology and Evolution",

issn = "1537-1719",

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Paulat, NS, Storer, JM, Moreno-Santillán, DD, Osmanski, AB, Sullivan, KAM, Grimshaw, JR, Korstian, J, Halsey, M, Garcia, CJ, Crookshanks, C, Roberts, J, Smit, AFA, Hubley, R, Rosen, J, Teeling, EC, Vernes, SC, Myers, E, Pippel, M, Brown, T, Hiller, M, Consortium, Z, Rojas, D, Dávalos, LM, Lindblad-Toh, K, Karlsson, EK & Ray, DA 2023, 'Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia', Molecular Biology and Evolution, vol. 40, no. 5, msad092. https://doi.org/10.1093/molbev/msad092

TY - JOUR

T1 - Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

AU - Paulat, Nicole S

AU - Storer, Jessica M

AU - Moreno-Santillán, Diana D

AU - Osmanski, Austin B

AU - Sullivan, Kevin A M

AU - Grimshaw, Jenna R

AU - Korstian, Jennifer

AU - Halsey, Michaela

AU - Garcia, Carlos J

AU - Crookshanks, Claudia

AU - Roberts, Jaquelyn

AU - Smit, Arian F A

AU - Hubley, Robert

AU - Rosen, Jeb

AU - Teeling, Emma C

AU - Vernes, Sonja C

AU - Myers, Eugene

AU - Pippel, Martin

AU - Brown, Thomas

AU - Hiller, Michael

AU - Consortium, Zoonomia

AU - Rojas, Danny

AU - Dávalos, Liliana M

AU - Lindblad-Toh, Kerstin

AU - Karlsson, Elinor K

AU - Ray, David A

N1 - Funding: This project was supported by the National Science Foundation (grant numbers DEB 1838283 and IOS 2032006 to D.M.-S. and Dav.R. and DEB 1838273 and DGE 1633299 to L.D.), National Institutes of Health (grant numbers R01HG002939 and U24HG010136 to J.S., R.H., A.F.A.S., and Je.R.), NHGRI (grant number R01HG008742 to Z.C.), Irish Research Council (grant number IRCLA/ 2017/58 to E.T.), Science Foundation Ireland (grant number 19/FFP/6790 to E.T.), Max Planck Research Group awarded by the Max Planck Gesellschaft to S.V., Human Frontiers Science Program (grant number RGP0058/2016 to S.V.), UK Research and Innovation (grant number MR/T021985/1 to S.V.), and the Swedish Research Council Distinguished Professor Award to K.L.-T.

PY - 2023/5/1

Y1 - 2023/5/1

N2 - Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

AB - Horizontal transfer of transposable elements (TEs) is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of TEs at what appears to be a high rate compared with other mammals. We investigated the occurrence of horizontally transferred (HT) DNA transposons involving bats. We found over 200 putative HT elements within bats; 16 transposons were shared across distantly related mammalian clades, and 2 other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

KW - Fusogenic envelope protein

KW - Platypus

KW - Endogenous retrovirus

KW - Echidna

KW - Monotremes

U2 - 10.1093/molbev/msad092

DO - 10.1093/molbev/msad092

M3 - Article

SN - 1537-1719

VL - 40

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 5

M1 - msad092

ER -

Chiropterans are a hotspot for horizontal transfer of DNA transposons in mammalia

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Keywords

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Sonja Vernes UKRI Future Leaders: Mammalian vocal communication as a model for human language; from genes and brains to behaviour

Cite this